Cottonseed Meal Protein Isolate as a New Source of Alternative Proteins: A Proteomics Perspective
Abstract
:1. Introduction
2. Results
2.1. Overview of the Protein Extraction and Gossypol Removal Workflow to Produce Ultra-Low Gossypol CSMPI
2.2. Proteomics Analysis Identified More Proteins in CSMPI after Gossypol Removal Treatment
2.3. Gossypol Removal Treatment Does Not Affect the Protein Integrity of CSMPI
2.4. Digestibility Protein Profile and In Silico Allergenic Analysis Identified Potential Allergens in Post-Treated CSMPI Digested with Different Enzymes
3. Discussion
3.1. The Developed Protein Extraction Method and Gossypol Treatment Improve Protein Functionalities
3.2. More Low-Abundance Proteins Identified in Post-Treated CSMPI
3.3. Higher Nutritional Content in Post-Treated CSMPI
3.4. CSMPI Digestibility Profile through LC-MS/MS Analysis and Identification of Potential Allergen through In Silico Prediction Analysis
4. Materials and Methods
4.1. Extraction of Protein Isolate from Cottonseed Meal
4.2. Gossypol Removal Treatment
4.3. Extraction of Free and Total Gossypol from Pre-Treated and Post-Treated CSMPI
4.4. Detection of Gossypol Level Using High-Performance Liquid Chromatography (HPLC)
4.5. Water Absorption Capacity (WAC), Oil Absorption Capacity (OAC) and Water Solubility
4.6. Emulsifying Activity Index (EAI) and Emulsion Stability Index (ESI) Measurement
4.7. Foaming Capacity and Stability Measurement
4.8. Sodium Dodecyl Sulphate–Polyacrylamide Gel Electrophoresis (SDS-PAGE)
4.9. Amino Acid Analysis
4.10. In Vitro Digestibility Assay
4.11. LC-MS/MS Analysis
4.12. Database Search
4.13. Bioinformatics Analysis
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Shahbandeh, M. Global Cottonseed Meal and Oil Production from 2009/2010 to 2017/2018; US Department of Agriculture, Economic Research Service: Washington, DC, USA, 2020; p. III-2-4.
- Li, X.; Rezaei, R.; Li, P.; Wu, G. Composition of amino acids in feed ingredients for animal diets. Amino Acids 2011, 40, 1159–1168. [Google Scholar] [CrossRef] [PubMed]
- Reiser, R.; Fu, H.C. The Mechanism of Gossypol Detoxification by Ruminant Animals. J. Nutr. 1962, 76, 215–218. [Google Scholar] [CrossRef]
- Yu, F.; Moughant, P.J.; Barry, T.N.; McNabb, W.C. The effect of condensed tannins from heated and unheated cottonseed on the ileal digestibility of amino acids for the growing rat and pig. Br. J. Nutr. 1996, 76, 359–371. [Google Scholar] [CrossRef] [PubMed]
- Gadelha, I.C.N.; Fonseca, N.B.S.; Oloris, S.C.S.; Melo, M.M.; Soto-Blanco, B. Gossypol toxicity from cottonseed products. Sci. World J. 2014, 2014, 231635. [Google Scholar] [CrossRef]
- Yu, Z.-H.; Chan, H.C. Gossypol as a male antifertility agent-why studies should have been continued. Int. J. Androl. 1998, 21, 2–7. [Google Scholar] [CrossRef]
- Blackwelder, J.T.; Hopkins, B.A.; Diaz, D.E.; Whitlow, L.W.; Brownie, C. Milk Production and Plasma Gossypol of Cows Fed Cottonseed and Oilseed Meals with or Without Rumen-Undegradable Protein. J. Dairy Sci. 1998, 81, 2934–2941. [Google Scholar] [CrossRef]
- Fernandez, S.R.; Zhang, Y.E.; Parsons, C.M. Dietary Formulation with Cottonseed Meal on a Total Amino Acid Versus a Digestible Amino Acid Basis. Poult. Sci. 1995, 74, 1168–1179. [Google Scholar] [CrossRef]
- European Food Safety, A. Gossypol as undesirable substance in animal feed—Scientific Opinion of the Panel on Contaminants in the Food Chain. EFSA J. 2009, 7, 908. [Google Scholar] [CrossRef]
- Lusas, E.W.; Jividen, G.M. Glandless cottonseed: A review of the first 25 years of processing and utilization research. J. Am. Oil Chem. Soc. 1987, 64, 839–854. [Google Scholar] [CrossRef]
- Janga, M.R.; Pandeya, D.; Campbell, L.M.; Konganti, K.; Villafuerte, S.T.; Puckhaber, L.; Pepper, A.; Stipanovic, R.D.; Scheffler, J.A.; Rathore, K.S. Genes regulating gland development in the cotton plant. Plant Biotechnol. J. 2019, 17, 1142–1153. [Google Scholar] [CrossRef]
- Rathore, K.S.; Pandeya, D.; Campbell, L.M.; Wedegaertner, T.C.; Puckhaber, L.; Stipanovic, R.D.; Thenell, J.S.; Hague, S.; Hake, K. Ultra-Low Gossypol Cottonseed: Selective Gene Silencing Opens Up a Vast Resource of Plant-Based Protein to Improve Human Nutrition. Crit. Rev. Plant Sci. 2020, 39, 1–29. [Google Scholar] [CrossRef]
- Turnbull, C.; Lillemo, M.; Hvoslef-Eide, T.A.K. Global Regulation of Genetically Modified Crops Amid the Gene Edited Crop Boom—A Review. Front. Plant Sci. 2021, 12, 630396. [Google Scholar] [CrossRef]
- Cui, K.; Shoemaker, S.P. Public perception of genetically-modified (GM) food: A Nationwide Chinese Consumer Study. npj Sci. Food 2018, 2, 10. [Google Scholar] [CrossRef] [PubMed]
- Bonny, S. Why are most Europeans opposed to GMOs? Factors explaining rejection in France and Europe. Electron. J. Biotechnol. 2003, 6, 7–8. [Google Scholar]
- Zhang, Y.; Zhang, Z.; Dai, L.; Liu, Y.; Cheng, M.; Chen, L. Isolation and characterization of a novel gossypol-degrading bacteria Bacillus subtilis strain Rumen Bacillus Subtilis. Asian Australas J. Anim. Sci. 2018, 31, 63–70. [Google Scholar] [CrossRef] [PubMed]
- Zhang, W.-j.; Xu, Z.-r.; Sun, J.-y.; Yang, X. Effect of selected fungi on the reduction of gossypol levels and nutritional value during solid substrate fermentation of cottonseed meal. J. Zhejiang Univ. Sci. B 2006, 7, 690–695. [Google Scholar] [CrossRef] [PubMed]
- Dechary, J.M.; Kupperman, R.P.; Thurber, F.H.; Altschul, A.M. Removal of gossypol from cottonseed by solvent extraction procedures. J. Am. Oil Chem. Soc. 1952, 29, 339–341. [Google Scholar] [CrossRef]
- Pelitire, S.M.; Dowd, M.K.; Cheng, H.N. Acidic solvent extraction of gossypol from cottonseed meal. Anim. Feed Sci. Technol. 2014, 195, 120–128. [Google Scholar] [CrossRef]
- Kumar, M.; Potkule, J.; Patil, S.; Saxena, S.; Patil, P.G.; Mageshwaran, V.; Punia, S.; Varghese, E.; Mahapatra, A.; Ashtaputre, N.; et al. Extraction of ultra-low gossypol protein from cottonseed: Characterization based on antioxidant activity, structural morphology and functional group analysis. LWT 2021, 140, 110692. [Google Scholar] [CrossRef]
- Singh, S.; Sharma, S.K.; Kansal, S.K. Batch extraction of gossypol from cottonseed meal using mixed solvent system and its kinetic modeling. Chem. Eng. Commun. 2019, 206, 1608–1617. [Google Scholar] [CrossRef]
- Małecki, J.; Muszyński, S.; Sołowiej, B.G. Proteins in Food Systems—Bionanomaterials, Conventional and Unconventional Sources, Functional Properties, and Development Opportunities. Polymers 2021, 13, 2506. [Google Scholar] [CrossRef] [PubMed]
- Wakasa, Y.; Takaiwa, F. Seed Storage Proteins. In Brenner’s Encyclopedia of Genetics, 2nd ed.; Maloy, S., Hughes, K., Eds.; Academic Press: San Diego, CA, USA, 2013; pp. 346–348. [Google Scholar]
- Viana, P.; Lima, P.; Paim, T.; Souza, J.; Dantas, A.; Pereira, E.; Gonçalves, V.; McManus, C.; Abdalla, A.; Louvandini, H. Gossypol was not detected in the longissimus muscle of lambs fed several forms of cottonseed. Anim. Prod. Sci. 2014, 55, 812–817. [Google Scholar]
- Pojić, M.; Mišan, A.; Tiwari, B. Eco-innovative technologies for extraction of proteins for human consumption from renewable protein sources of plant origin. Trends Food Sci. Technol. 2018, 75, 93–104. [Google Scholar]
- Martínez-Maqueda, D.; Hernández-Ledesma, B.; Amigo, L.; Miralles, B.; Gómez-Ruiz, J.Á. Extraction/fractionation techniques for proteins and peptides and protein digestion. In Proteomics in Foods; Springer: New York, NY, USA, 2013; pp. 21–50. [Google Scholar]
- Zhang, C.; Sanders, J.P.; Xiao, T.T.; Bruins, M.E. How does alkali aid protein extraction in green tea leaf residue: A basis for integrated biorefinery of leaves. PLoS ONE 2015, 10, e0133046. [Google Scholar]
- EFSA Panel on Contaminants in the Food Chain; Knutsen, H.K.; Barregård, L.; Bignami, M.; Brüschweiler, B.; Ceccatelli, S.; Dinovi, M.; Edler, L.; Grasl-Kraupp, B.; Hogstrand, C.; et al. Presence of free gossypol in whole cottonseed. EFSA J. 2017, 15, e04850. [Google Scholar] [CrossRef]
- Adebowale, Y.; Adeyemi, I.; Oshodi, A. Functional and physicochemical properties of flours of six Mucuna species. Afr. J. Biotechnol. 2005, 4, 1461–1468. [Google Scholar]
- Ma, M.; Ren, Y.; Xie, W.; Zhou, D.; Tang, S.; Kuang, M.; Wang, Y.; Du, S.-k. Physicochemical and functional properties of protein isolate obtained from cottonseed meal. Food Chem. 2018, 240, 856–862. [Google Scholar] [CrossRef]
- Zayas, J.F. Oil and Fat Binding Properties of Proteins. In Functionality of Proteins in Food; Zayas, J.F., Ed.; Springer: Berlin/Heidelberg, Germany, 1997; pp. 228–259. [Google Scholar]
- He, Z.; Zhang, D.; Cao, H. Protein profiling of water and alkali soluble cottonseed protein isolates. Sci. Rep. 2018, 8, 9306. [Google Scholar] [CrossRef]
- Fernandez, S.R.; Parsons, C.M. Bioavailability of the Digestible Lysine and Valine in Cottonseed and Soybean Meals for Chicks. Poult. Sci. 1996, 75, 216–223. [Google Scholar] [CrossRef]
- Ma, X.; Hu, J.; Shang, Q.; Liu, H.; Piao, X. Chemical composition, energy content and amino acid digestibility in cottonseed meals fed to growing pigs. J. Appl. Anim. Res. 2019, 47, 280–288. [Google Scholar] [CrossRef]
- Kimball, S.R.; Jefferson, L.S. Signaling Pathways and Molecular Mechanisms through which Branched-Chain Amino Acids Mediate Translational Control of Protein Synthesis. J. Nutr. 2006, 136, 227S–231S. [Google Scholar] [CrossRef] [PubMed]
- Kim, D.-H.; Kim, S.-H.; Jeong, W.-S.; Lee, H.-Y. Effect of BCAA intake during endurance exercises on fatigue substances, muscle damage substances, and energy metabolism substances. J. Exerc. Nutr. Biochem. 2013, 17, 169–180. [Google Scholar] [CrossRef] [PubMed]
- Rondanelli, M.; Faliva, M.; Monteferrario, F.; Peroni, G.; Repaci, E.; Allieri, F.; Perna, S. Novel Insights on Nutrient Management of Sarcopenia in Elderly. BioMed Res. Int. 2015, 2015, 524948. [Google Scholar] [CrossRef] [PubMed]
- Kamei, Y.; Hatazawa, Y.; Uchitomi, R.; Yoshimura, R.; Miura, S. Regulation of Skeletal Muscle Function by Amino Acids. Nutrients 2020, 12, 261. [Google Scholar]
- Sun, X.D. Enzymatic hydrolysis of soy proteins and the hydrolysates utilisation. Int. J. Food Sci. Technol. 2011, 46, 2447–2459. [Google Scholar]
- Erickson, R.H.; Kim, Y.S. Digestion and absorption of dietary protein. Annu. Rev. Med. 1990, 41, 133–139. [Google Scholar] [CrossRef]
- Joye, I. Protein Digestibility of Cereal Products. Foods 2019, 8, 199. [Google Scholar] [CrossRef] [Green Version]
- EFSA Panel on Genetically Modified Organisms; Naegeli, H.; Bresson, J.-L.; Dalmay, T.; Dewhurst, I.C.; Epstein, M.M.; Firbank, L.G.; Guerche, P.; Hejatko, J.; Moreno, F.J.; et al. Statement on in vitro protein digestibility tests in allergenicity and protein safety assessment of genetically modified plants. EFSA J. 2021, 19, e06350. [Google Scholar] [CrossRef]
- Pali-Schöll, I.; Untersmayr, E.; Klems, M.; Jensen-Jarolim, E. The Effect of Digestion and Digestibility on Allergenicity of Food. Nutrients 2018, 10, 1129. [Google Scholar] [CrossRef]
- Verhoeckx, K.; Bøgh, K.L.; Dupont, D.; Egger, L.; Gadermaier, G.; Larré, C.; Mackie, A.; Menard, O.; Adel-Patient, K.; Picariello, G.; et al. The relevance of a digestibility evaluation in the allergenicity risk assessment of novel proteins. Opinion of a joint initiative of COST action ImpARAS and COST action INFOGEST. Food Chem. Toxicol. 2019, 129, 405–423. [Google Scholar] [CrossRef]
- Pekar, J.; Ret, D.; Untersmayr, E. Stability of allergens. Mol. Immunol. 2018, 100, 14–20. [Google Scholar] [CrossRef] [PubMed]
- Verhoeckx, K.C.M.; Vissers, Y.M.; Baumert, J.L.; Faludi, R.; Feys, M.; Flanagan, S.; Herouet-Guicheney, C.; Holzhauser, T.; Shimojo, R.; van der Bolt, N.; et al. Food processing and allergenicity. Food Chem. Toxicol. 2015, 80, 223–240. [Google Scholar] [CrossRef] [PubMed]
- Food and Agriculture Organization of the United Nations. Evaluation of Allergenicity of Genetically Modified Foods: Report of a Joint FAO/WHO Expert Consultation on Allergenicity of Foods Derived from Biotechnology, 22–25 January 2001; Food and Agriculture Organization of the United Nations: Rome, Italy, 2001. [Google Scholar]
- Abdelmoteleb, M.; Zhang, C.; Furey, B.; Kozubal, M.; Griffiths, H.; Champeaud, M.; Goodman, R.E. Evaluating potential risks of food allergy of novel food sources based on comparison of proteins predicted from genomes and compared to www.AllergenOnline.org. Food Chem. Toxicol. 2021, 147, 111888. [Google Scholar] [CrossRef] [PubMed]
- Halima, O.; Najar, F.Z.; Wahab, A.; Gamagedara, S.; Chowdhury, A.I.; Foster, S.B.; Shaheen, N.; Ahsan, N. Lentil allergens identification and quantification: An update from omics perspective. Food Chem. Mol. Sci. 2022, 4, 100109. [Google Scholar] [CrossRef] [PubMed]
- Nguyen, M.N.; Krutz, N.L.; Limviphuvadh, V.; Lopata, A.L.; Gerberick, G.F.; Maurer-Stroh, S. AllerCatPro 2.0: A web server for predicting protein allergenicity potential. Nucleic Acids Res. 2022, 50, W36–W43. [Google Scholar] [CrossRef]
- Burks, A.W.; Williams, L.W.; Thresher, W.; Connaughton, C.; Cockrell, G.; Helm, R.M. Allergenicity of peanut and soybean extracts altered by chemical or thermal denaturation in patients with atopic dermatitis and positive food challenges. J. Allergy Clin. Immunol. 1992, 90, 889–897. [Google Scholar] [CrossRef]
- Atkins, F.M.; Wilson, M.; Bock, S.A. Cottonseed hypersensitivity: New concerns over an old problem. J. Allergy Clin. Immunol. 1988, 82, 242–250. [Google Scholar] [CrossRef]
- Malanin, G.; Kalimo, K. Angioedema and urticaria caused by cottonseed protein in whole-grain bread. J. Allergy Clin. Immunol. 1988, 82, 261–264. [Google Scholar] [CrossRef]
- Singh, P.; Arora, A.; Strand, T.A.; Leffler, D.A.; Catassi, C.; Green, P.H.; Kelly, C.P.; Ahuja, V.; Makharia, G.K. Global Prevalence of Celiac Disease: Systematic Review and Meta-analysis. Clin. Gastroenterol. Hepatol. 2018, 16, 823–836.e822. [Google Scholar] [CrossRef]
- Cabanillas, B.; Jappe, U.; Novak, N. Allergy to Peanut, Soybean, and Other Legumes: Recent Advances in Allergen Characterization, Stability to Processing and IgE Cross-Reactivity. Mol. Nutr. Food Res. 2018, 62, 1700446. [Google Scholar] [CrossRef]
- Bradford, M.M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 1976, 72, 248–254. [Google Scholar] [CrossRef]
- Conceição, A.A.; Soares Neto, C.B.; Ribeiro, J.A.d.A.; Siqueira, F.G.d.; Miller, R.N.G.; Mendonça, S. Development of an RP-UHPLC-PDA method for quantification of free gossypol in cottonseed cake and fungal-treated cottonseed cake. PLoS ONE 2018, 13, e0196164. [Google Scholar] [CrossRef]
- Kraithong, S.; Lee, S.; Rawdkuen, S. Physicochemical and functional properties of Thai organic rice flour. J. Cereal Sci. 2018, 79, 259–266. [Google Scholar]
- Cameron, D.R.; Weber, M.E.; Idziak, E.S.; Neufeld, R.J.; Cooper, D.G. Determination of interfacial areas in emulsions using turbidimetric and droplet size data: Correction of the formula for emulsifying activity index. J. Agric. Food Chem. 1991, 39, 655–659. [Google Scholar] [CrossRef]
- Xue, G.; Ren, D.; Zhou, C.; Zheng, H.; Cao, W.; Lin, H.; Qin, X.; Zhang, C. Comparative study on the functional properties of the pearl oyster (Pinctada martensii) protein isolates and its electrostatic complexes with three hydrophilic polysaccharides. Int. J. Food Prop. 2020, 23, 1256–1271. [Google Scholar] [CrossRef]
- Chao, D.; Aluko, R.E. Modification of the structural, emulsifying, and foaming properties of an isolated pea protein by thermal pretreatment. CyTA J. Food 2018, 16, 357–366. [Google Scholar] [CrossRef]
- Waters-Corporation. AccQ-Tag Ultra Derivatization Kit Care and Use User Manual. Available online: https://www.waters.com/webassets/cms/support/docs/715001331.pdf (accessed on 20 August 2022).
- Wiśniewski, J.R.; Zougman, A.; Nagaraj, N.; Mann, M. Universal sample preparation method for proteome analysis. Nat. Methods 2009, 6, 359–362. [Google Scholar] [CrossRef] [PubMed]
- Sim, K.H.; Liu, L.C.-Y.; Tan, H.T.; Tan, K.; Ng, D.; Zhang, W.; Yang, Y.; Tate, S.; Bi, X. A comprehensive CHO SWATH-MS spectral library for robust quantitative profiling of 10,000 proteins. Sci. Data 2020, 7, 263. [Google Scholar] [CrossRef]
- Minkiewicz, P.; Iwaniak, A.; Darewicz, M. BIOPEP-UWM database of bioactive peptides: Current opportunities. Int. J. Mol. Sci. 2019, 20, 5978. [Google Scholar] [CrossRef]
- Gu, Z.; Eils, R.; Schlesner, M. Complex heatmaps reveal patterns and correlations in multidimensional genomic data. Bioinformatics 2016, 32, 2847–2849. [Google Scholar] [CrossRef]
- Perez-Riverol, Y.; Csordas, A.; Bai, J.; Bernal-Llinares, M.; Hewapathirana, S.; Kundu, D.J.; Inuganti, A.; Griss, J.; Mayer, G.; Eisenacher, M.; et al. The PRIDE database and related tools and resources in 2019: Improving support for quantification data. Nucleic Acids Res. 2019, 47, D442–D450. [Google Scholar] [CrossRef] [PubMed]
CSMPI | PPI | |
---|---|---|
Water absorption capacity (WAC) (mg/mg) | 3.27 ± 0.03 *** | 4.41 ± 0.09 |
Oil absorption capacity (OAC) (mg/mg) | 2.90 ± 0.06 *** | 2.26 ± 0.02 |
Water solubility (%) | 47.53 ± 3.12 * | 37.28 ± 0.04 |
Emulsifying activity index (EAI) (m2/g) | 4.15 ± 0.27 ** | 11.59 ± 1.19 |
Emulsion stability index (ESI) (min) | 115.93 ± 7.13 | 183.60 ± 44.90 |
Foaming capacity (FC) (%) | 27.05 ± 1.43 | 23.70 ± 0.44 |
Foaming stability (FS) (%) | 96.13 ± 0.05 | 96.77 ± 1.70 |
Time (min) | Aqueous-0.1% TFA (%) | Organic-Methanol (%) |
---|---|---|
0 | 40 | 60 |
8 | 0 | 100 |
11 | 0 | 100 |
12.5 | 40 | 60 |
16.5 | 40 | 60 |
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations. |
© 2022 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Tan, C.F.; Kwan, S.H.; Lee, C.S.; Soh, Y.N.A.; Ho, Y.S.; Bi, X. Cottonseed Meal Protein Isolate as a New Source of Alternative Proteins: A Proteomics Perspective. Int. J. Mol. Sci. 2022, 23, 10105. https://doi.org/10.3390/ijms231710105
Tan CF, Kwan SH, Lee CS, Soh YNA, Ho YS, Bi X. Cottonseed Meal Protein Isolate as a New Source of Alternative Proteins: A Proteomics Perspective. International Journal of Molecular Sciences. 2022; 23(17):10105. https://doi.org/10.3390/ijms231710105
Chicago/Turabian StyleTan, Chee Fan, Soon Hong Kwan, Chun Shing Lee, Yan Ni Annie Soh, Ying Swan Ho, and Xuezhi Bi. 2022. "Cottonseed Meal Protein Isolate as a New Source of Alternative Proteins: A Proteomics Perspective" International Journal of Molecular Sciences 23, no. 17: 10105. https://doi.org/10.3390/ijms231710105